Effects of Probiotic Treated Pomegranate Residue on Growth Performance, Immunity and Microbiome in the Intestines of Broilers
DOI:
https://doi.org/10.3923/ijps.2001.37.45Keywords:
Broiler, immunity, intestinal microbiology, pomegranate residue, probioticsAbstract
Objectives: This research was undertaken to assess the effect of probiotic treated pomegranate residue (PPR) on growth performance, serum immunoglobulins, intestinal and excreta microbiome, and excreta harmful gas emission in broilers. Materials and Methods: A total of 128 day-old Ross-308 chicks were randomly assigned to 4 treatment groups, each consisting of 4 replicates of 8 birds. The experimental diets were formulated to supply 0, 0.5, 1.0 and 2.0% of PPR and were fed for 35 day. Results: Dietary inclusion of PPR linearly increased the weight gain of broiler, while reduced FCR by almost 0.10 points without affecting the feed intake (p<0.05). Following the addition of PPR, a linear rise in serum IgA concentration was perceived (p<0.05). Dietary PPR increased the ileal and cecal Lactobacillus, cecal Bacillus (linear, p<0.05) and ileal yeast and mold (linear, p = 0.0007; quadratic, p = 0.007) population. In contrary, the E. coli population has been decreased in the ileal (linear, p = 0.004, quadratic, p<0.04) and cecal digesta (linear, p = 0.004) and Salmonella only in the cecal digesta (linear, p = 0.0004) in consequence of dietary PPR. As the dose level increased PPR linearly reduced the ileal and cecal pH (p<0.05). Dietary PPR increased the CFU of excreta Lactobacillus (linear, p = 0.002) and Bacillus (quadratic, p<0.05), whereas, decreased the E. coli population (linear, p = 0.008). In relation to dietary PPR supplementation, excreta pH was linearly lowered (p<0.05). Inclusion of 1% and 2% PPR reduced the NH3 and H2S emission from broiler excreta. Conclusion: Therefore, it can be concluded that PPR supplemented up to 2% level may improve the growth performance, immunity and microbiome in the intestines of broilers.
References
Viveros, A., S. Chamorro, M. Pizarro, I. Arija, C. Centeno and A. Brenes, 2011. Effects of dietary polyphenol-rich grape products on intestinal microflora and gut morphology in broiler chicks. Poult. Sci., 90: 566-578.
Shabtay, A., H. Eitam, Y. Tadmor, A. Orlov and A. Meir et al., 2008. Nutritive and antioxidative potential of fresh and stored pomegranate industrial byproduct as a novel beef cattle feed. J. Agric. Food Chem., 56: 10063-10070.
Seeram, N.P., L.S. Adams, S.M. Henning, Y. Niu, Y. Zhang, M.G. Nair and D. Heber, 2005. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem., 16: 360-367.
Ross, R.G., S. Selvasubramanian and S. Jayasundar, 2001. Immunomodulatory activity of Punica granatum in rabbits-a preliminary study. J. Ethnopharmacol., 78: 85-87.
Kanatt, S.R., R. Chander and A. Sharma, 2010. Antioxidant and antimicrobial activity of pomegranate peel extract improves the shelf life of chicken products. Int. J. Food Sci. Technol., 45: 216-222.
Oboh, G., K.B. Alabi and A.A. Akindahunsi, 2008. Fermentation changes the nutritive value, polyphenol distribution, and antioxidant properties of Parkia biglobosa seeds (African locust beans). Food Biotechnol., 22: 363-376.
Hong, K.J., C.H. Lee and S.W. Kim, 2004. Aspergillus oryzae GB-107 Fermentation improves nutritional quality of food soybeans and feed soybean meals. J. Med. Food, 7: 430-435.
Venugopalan, V., K.A. Shriner and A. Wong-Beringer, 2010. Regulatory oversight and safety of probiotic use. Emerging Infect. Dis., 16: 1661-1665.
Hossain, M.E and C.J. Yang, 2014. Effect of fermented water plantain on growth performance, meat composition, oxidative stability, and fatty acid composition of broiler. Livestock Sci., 162: 168-177.
Hossain, M.E., S.Y. Ko, G.M. Kim, J.D. Firman and C.J. Yang, 2012. Evaluation of probiotic strains for development of fermented Alisma canaliculatum and their effects on broiler chickens. Poult. Sci., 91: 3121-3131.
Ahmed, S.T., S. ,Y Ko and C. ,J Yang, 2017. Improving the nutritional quality and shelf life of broiler meat by feeding diets supplemented with fermented pomegranate (Punica granatum L.) by-products. Br. Poult. Sci., 58: 694-703.
AOAC., 1995. Official Methods of Analysis. 16th Edn., Association of Official Analytical Chemists, Washington, DC, USA.
NRC., 1994. Nutrient Requirements of Poultry. 9th Edn., National Academy Press, Washington, DC., USA., ISBN-13: 9780309048927, Pages: 176.
Ahmed, S.T. and C.J. Yang, 2017. Effects of dietary Punica granatum L. by-products on performance, immunity, intestinal and fecal microbiology and odorous gas emissions from excreta in broilers. J. Poult. Sci., 54: 157-166.
SAS Institute Inc., 2011. SAS/STAT® 9.3 User's Guide. SAS Institute Inc., Cary, NC, Pages: 8285.
Armstrong, W.D., W.R. Featherston and J.C. Rogler, 1974. Effects of bird resistant sorghum grain and various commercial tannins on chick performance. Poult. Sci., 53: 2137-2142.
Smulikowska, S., B. Pastuszewska, E. Święch, A. Ochtabińska, A. Mieczkowska, V. Nguyen and L. Buraczewska, 2017. Tannin content affects negatively nutritive value of pea for monogastrics. J. Anim. Feed Sci., 10: 511-523.
Reddy, N.R. and M.D. Pierson, 1994. Reduction in antinutritional and toxic components in plant foods by fermentation. Food Res. Int., 27: 281-290.
Dei, H.K., S.P. Rose, A.M. Mackenzie and R. Amarowicz, 2008. Growth performance of broiler chickens fed diets containing shea nut (Vitellaria paradoxa, Gaertn.) meal fermented with Aspergillus niger. Poult. Sci., 87: 1773-1778.
Mondal, K.C., D. Banerjee, M. Jana and B.R. Pati, 2001. Colorimetric assay method for determination of the tannin acyl hydrolase (EC 3.1.1.20) activity. Anal. Biochem., 295: 168-171.
Mondal, K.C., D. Banerjee, R. Banerjee and B.R. Pati, 2001. Production and characterization of tannase from Bacillus cereus KBR9. J. Gen. Applied Microbiol., 47: 263-267.
Feng, J., X. Liu, Z.R. Xu, Y.Y. Liu and Y.P. Lu, 2007. Effects of Aspergillus oryzae 3.042 fermented soybean meal on growth performance and plasma biochemical parameters in broilers. Anim. Feed Sci. Technol., 134: 235-242.
Lee, H.S., M.R. Kim, Y. Park, H.J. Park, U.J. Chang, S.Y. Kim and H.J. Suh, 2012. Fermenting red ginseng enhances its safety and efficacy as a novel skin care anti-aging ingredient: In vitro and animal study. J. Medic. Food, 15: 1015-1023.
Chen, K.L., W.L. Kho, S.H. You, R.H. Yeh, S.W. Tang and C.W. Hsieh, 2009. Effects of Bacillus subtilis var. natto and Saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers. Poult. Sci., 88: 309-315.
Yamasaki, M., T. Kitagawa, N. Koyanagi, H. Chujo and H. Maeda et al., 2005. Dietary effect of pomegranate seed oil on immune function and lipid metabolism in mice. Nutrition, 22: 54-59.
Nuamsetti, T., P. Dechayuenyong and S. Tantipaibulvut, 2012. Antibacterial activity of pomegranate fruit peels and arils. ScienceAsia, 38: 319-322.
Kışla, D. and Ş. Karabıyıklı, 2013. Antimicrobial effect of sour pomegranate sauce on Escherichia coli O157 : H7 and Staphylococcus aureus. J. Food Sci., Vol. 78.
Filannino, P., L. Azzi, I. Cavoski, O. Vincentini, C.G. Rizzello, M. Gobbetti and R.D. Cagno, 2013. Exploitation of the health-promoting and sensory properties of organic pomegranate (Punica granatum L.) juice through lactic acid fermentation. Int. J. Food Microbiol., 163: 184-192.
Hosoi, T., A. Ametani, K. Kiuchi and S. Kaminogawa, 2011. Improved growth and viability of lactobacilli in the presence of Bacillus subtilis (natto), catalase, or subtilisin. Can. J. Microbiol., 46: 892-897.
Hayek, S.A. and S.A. Ibrahim, 2013. Current limitations and challenges with lactic acid bacteria: A review. Food Nutr. Sci., 4: 73-87.
Ferket, P.R., E. van Heugten, T.A.T.G. van Kempen and R. Angel, 2017. Nutritional strategies to reduce environmental emissions from nonruminants. J. Anim. Sci., Vol. 80.
Wrong, O.M., 1981. Nitrogen Compounds. In: The Large Intestine: Its Role in Mammalian Nutrition and Homeostasis, Wrong, O.M., C.J. Edmonds and V.S. Chadwick., (Eds.). Wiley and Sons, New York, USA, pp: 133-211.
Yeo, J. and K.I. Kim, 1997. Effect of feeding diets containing an antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks. Poult. Sci., 76: 381-385.
Endo, T., M. Nakaro, S. Shimizu, M. Fukushima and S. Miyoshi, 1999. Effects of a probiotic on the lipid metabolism of cocks fed on a cholesterol-enriched diet. Biosci. Biotechnol. Biochem., 63: 1569-1575.
Arogo, J., R.H. Zhang, G.L. Riskowski and D.L. Day, 2013. Hydrogen sulfide production from stored liquid swine manure: A laboratory study. Trans. ASAE, 43: 1241-1245.
Maker, M.D. and J.A. Washington, 2020. Hydrogen sulfide-producing variants of Escherichia coli. Applied Microbiol., 28: 303-305.
USHIDA, K., N. OSHIMA, A. TANIMURA, K. MIYAZAKI, Y. KOJIMA and S. TAKAKUWA, 2014. Evaluation of methanethiol and hydrogen sulfide production by standard strains of intestinal bacteria and isolates from pig feces. Biosci. Microflora, 20: 53-57.
Downloads
Published
Issue
Section
License
Copyright (c) 2025 The Author(s)

This work is licensed under a Creative Commons Attribution 4.0 International License.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.